Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium

Journal of Biogeography

Volumn 37, Issue 5, 2010, Pages 785-800

  LaJeunesse, Todd C ^a   Pettay, Daniel T ^a   Sampayo, Eugenia M ^a   Phongsuwan, Niphon ^b   Brown, Barbara ^c   Obura, David O ^d   Hoegh Guldberg, Ove ^e   Fitt, William K ^f  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PHUKET MARINE BIOLOGICAL CENTER   (Thailand)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d Coastal Ocean Research and Development Indian Ocean CORDIO ^*  (Kenya)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

Adaptive radiation; Andaman Sea; Dinoflagellate endosymbionts; Great Barrier Reef; Indian Ocean; Reef corals; Symbiodinium; Zanzibar

Indexed keywords

ADAPTIVE RADIATION; CLIMATE CHANGE; CORAL REEF; DINOFLAGELLATE; DOMINANCE; ENDOSYMBIONT; ENVIRONMENTAL CONDITIONS; GENETIC MARKER; GENETIC VARIATION; HOST-SYMBIONT INTERACTION; ISOLATED POPULATION; PHYLOGENETICS; PHYLOGEOGRAPHY; PLEISTOCENE; SPECIES DIVERSITY;

AUSTRALIA; CORAL SEA; GREAT BARRIER REEF; INDIAN OCEAN; PACIFIC OCEAN; QUEENSLAND;

ALGAE; ANTHOZOA; DINOPHYCEAE; INVERTEBRATA; SYMBIODINIUM;

EID: 77953098950     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2010.02273.x     Document Type: Article

References (89)

1. Alverson AJ. Molecular systematics and the diatom species. Protist 2008, 159:339-353.
2. Baird AH, Marshall PA. Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Marine Ecology Progress Series 2002, 237:133-141.
3. Baker AC. Flexibility and specificity in coral-algal symbiosis: diversity, ecology and biogeography of Symbiodinium. Annual Review of Ecology Evolution and Systematics 2003, 34:661-689.
4. Baker AC, Starger CJ, McClanahan TR, Glynn PW. Corals' adaptive response to climate change. Nature 2004, 430:741.
5. Benzie JAH. Genetic structure of coral reef organisms: ghosts of dispersal past. American Zoologist 1999, 39:131-145.
6. Berkelmans R, Oliver J. Large-scale bleaching of corals on the Great Barrier Reef. Coral Reefs 1999, 18:55-60.
7. Berkelmans R, van Oppen MJH. The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change. Proceedings of the Royal Society B: Biological Sciences 2006, 273:2305-2312.
8. Berkelmans R, De'ath G, Kininmonth S, Skirving W. A comparison of the 1998 and 2002 coral bleaching events on the Great Barrier Reef: spatial correlation, patterns and predictions. Coral Reefs 2004, 23:74-84.
9. Bray JR, Curtis JT. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 1957, 27:325-349.
10. Brown BE. Coral bleaching: causes and consequences. Coral Reefs 1997, 16:S129-S138.
11. Brown BE. Coral reefs of the Andaman Sea: an integrated perspective. Oceanography and Marine Biology: an Annual Review 2007, 45:173-194.
12. Brown BE, Phongsuwan N. Constancy and change on shallow reefs around Laem Pan Wa, Phuket, Thailand over a twenty year period. Phuket Marine Biology Center Research Bulletin 2004, 65:61-73.
13. Burnett WJ. Longitudinal variation in algal symbionts (zooxanthellae) from the Indian Ocean zoanthid Palythoa caesia. Marine Ecology Progress Series 2002, 234:105-109.
14. Chen CA, Yang YW, Wei NV, Tsai WS, Fang LS. Symbiont diversity in scleractinian corals from tropical reefs and subtropical non-reef communities in Taiwan. Coral Reefs 2005, 24:11-22.
15. Coffroth MA, Santos SR. Genetic diversity of symbiotic dinoflagellates in the genus Symbiodinium. Protist 2005, 156:19-34.
16. Coles SL. Reef corals occurring in a highly fluctuating temperature environment at Fahal Island, Gulf of Oman (Indian Ocean). Coral Reefs 1997, 16:269-272.
17. Dove S, Ortiz JC, Enriquez S, Fine M, Fisher P, Igelsias-Prieto R, Thornhill D, Hoegh-Guldberg O. Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short term heat stress. Limnology and Oceanography 2006, 51:1149-1158.
18. Dover GA. Molecular drive: a cohesive mode of species evolution. Nature 1982, 299:111-117.
19. Dunne RP, Brown BE. Penetration of solar UVB radiation in shallow tropical waters and its potential biological effect on coral reefs: results from the central Indian Ocean and Andaman Sea. Marine Ecology Progress Series 1996, 144:109-118.
20. Fabricius KE, Mieog JC, Colin PL, Idip D, van Oppen MJH. Identity and diversity of coral endosymbionts (zooxanthellae) from three Palauan reefs with contrasting bleaching, temperature and shading histories. Molecular Ecology 2004, 13:2445-2458.
21. Fisher P. Investigating the photo-physiology of Symbiodinium sub-clades and its relationship to coral bleaching 2006, PhD Thesis, Centre for Marine Studies, University of Queensland, Brisbane, Australia
22. Fitt WK, Brown BE, Warner ME, Dunne RP. Coral bleaching: interpretation of thermal tolerance limits and thermal thresholds in tropical corals. Coral Reefs 2001, 20:51-65.
23. Frade PR, de Jongh F, Vermeulen F, van Bleijswijk J, Bak RPM. Variation in symbiont distribution between closely related coral species over large depth ranges. Molecular Ecology 2008, 17:691-703.
24. Futuyma DJ, Moreno G. The evolution of ecological specialization. Annual Reviews in Ecology and Systematics 1988, 19:207-233.
25. Garren M, Walsh SM, Caccone A, Knowlton N. Patterns of association between Symbiodinium and members of the Montastraea annularis species complex on spatial scales ranging from within colonies to between geographic regions. Coral Reefs 2006, 25:503-512.
26. Glynn PW. Coral bleaching: ecological perspectives. Coral Reefs 1993, 12:1-17.
27. Goulet TL, LaJeunesse TC, Fabricius K. Symbiont specificity and bleaching susceptibility among soft corals during the 1998 GBR mass coral bleaching event. Marine Biology 2008, 154:795-804.
28. Hansen G, Daugbjerg N. Symbiodinium natans sp. nov.: a 'free-living' dinoflagellate from Tenerife (northwest-Atlantic Ocean). Journal of Phycology 2009, 45:251-263.
29. Hoegh-Guldberg O. Climate change, coral bleaching and the future of the world's coral reefs. Journal of Marine and Freshwater Research 1999, 50:839-866.
30. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME. Coral reefs under rapid climate change and ocean acidification. Science 2007, 318:1737-1742.
31. Huelsenbeck JP, Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
32. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J. Climate change, human impacts, and the resilience of coral reefs. Science 2003, 301:929-933.
33. Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society B: Biological Sciences 2004, 271:1757-1763.
34. Jones AM, Berkelmans R, van Oppen MJH, Mieog JC, Sinclair W. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proceedings of the Royal Society B: Biological Sciences 2008, 275:1359-1365.
35. LaJeunesse TC. Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Marine Biology 2002, 141:387-400.
36. LaJeunesse TC. 'Species' radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Molecular Biology and Evolution 2005, 22:570-581.
37. LaJeunesse TC, Trench RK. Biogeography of two species of Symbiodinium (Freudenthal) inhabiting the intertidal sea anemone Anthopleura elegantissima (Brandt). Biological Bulletin 2000, 199:126-134.
38. LaJeunesse TC, Loh WKW, van Woesik R, Hoegh-Guldberg O, Schmidt GW, Fitt WK. Low symbiont diversity in southern Great Barrier Reef corals relative to those of the Caribbean. Limnology and Oceanography 2003, 48:2046-2054.
39. LaJeunesse TC, Bhagooli R, Hidaka M, deVantier L, Done T, Schmidt GW, Fitt WK, Hoegh-Guldberg O. Closely related Symbiodinium spp. differ in relative dominance in coral reef host communities across environmental, latitudinal and biogeographic gradients. Marine Ecology Progress Series 2004a, 284:147-161.
40. LaJeunesse TC, Thornhill DJ, Cox E, Stanton F, Fitt WK, Schmidt GW. High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii. Coral Reefs 2004b, 23:596-603.
41. LaJeunesse TC, Lambert G, Andersen RA, Coffroth MA, Galbraith DW. Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. Journal of Phycology 2005, 41:880-886.
42. LaJeunesse TC, Reyes-Bonilla H, Warner ME. Spring 'bleaching' among Pocillopora in the Sea of Cortez, Eastern Pacific. Coral Reefs 2007, 26:265-270.
43. LaJeunesse TC, Reyes-Bonilla H, Warner ME, Wills M, Schmidt GW, Fitt WK. Specificity and stability in high latitude eastern Pacific coral-algal symbioses. Limnology and Oceanography 2008, 53:719-727.
44. LaJeunesse TC, Smith RT, Finney J, Oxenford H. Outbreak and persistence of opportunistic symbiotic dinoflagellates during the 2005 Caribbean mass coral 'bleaching' event. Proceedings of the Royal Society B: Biological Sciences 2009, 276:4139-4148.
45. Lien YT, Nakano Y, Plathong S, Fukami H, Wang JT, Chen CA. Occurrence of the putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal marginal coral communities. Coral Reefs 2007, 26:35-44.
46. Litaker RW, Vandersea MW, Reece KS, Stokes NA, Yonish BA, Kibler SR, Black MND, Steidinger KA, Lutzoni FM, Tester PA. Recognizing dinoflagellate species using ITS rDNA sequences. Journal of Phycology 2007, 43:344-355.
47. Loh WKW, Loi T, Carter D, Hoegh-Guldberg O. Genetic variability of the symbiotic dinoflagellates from the wide ranging coral species Seriatopora hystrix and Acropora longicyathus in the Indo-West Pacific. Marine Ecology Progress Series 2001, 222:97-107.
48. MacDonald AHH, Sampayo EM, Ridgway T, Schleyer MH. Latitudinal symbiont zonation in Stylophora pistillata from southeast Africa. Marine Biology 2008, 154:209-217.
49. McClanahan TR, Maina J, Moothien-Pillay KR, Baker AC. Effects of geography, taxa, water flow, and temperature variation on coral bleaching intensity in Mauritius. Marine Ecology Progress Series 2005, 298:131-142.
50. Mostafavi PG, Fatemi SMR, Shahhosseiny MH, Hoegh-Guldberg O, Loh WKW. Predominance of Clade D Symbiodinium in shallow-water reef-building corals off Kish and Larak Islands (Persian Gulf, Iran). Marine Biology 2007, 153:25-34.
51. Myers RM, Sheffield VC, Cox DR. Mutation detection by PCR GC-clamps, and denaturing gradient gel electrophoresis. PCR-technology principles and applications for DNA amplification 1989, 71-88. Erlich HA, ed. by, pp, Stockton Press, New York
52. van Oppen MJH, Mahini AJ, Done TJ. Geographic distribution of zooxanthella types in three coral species on the Great Barrier Reef sampled after the 2002 bleaching event. Coral Reefs 2005a, 24:482-487.
53. van Oppen MJH, Mieog JC, Sánchez A, Fabricius KE. Diversity of algal endosymbionts (zooxanthellae) in octocorals: the roles of geography and host relationships. Molecular Ecology 2005b, 14:2403-2417.
54. Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 2006, 6:288-295.
55. Pettay DT, LaJeunesse TC. Microsatellite loci for assessing genetic diversity, dispersal and clonality of coral symbionts in 'stress-tolerant' Clade D Symbiodinium. Molecular Ecology Resources 2009, 9:1022-1025.
56. Pochon X, LaJeunesse TC, Pawlowski J. Biogeographic partitioning and host specialization among foraminiferan dinoflagellate symbionts (Symbiodinium, Dinophyta). Marine Biology 2004, 146:17-27.
57. Pochon X, Garcia-Cuestos L, Baker AC, Castella E, Pawlowski J. One-year survey of a single Micronesian reef reveals extraordinarily rich diversity of Symbiodinium types in soritid foraminifera. Coral Reefs 2007, 26:867-882.
58. Potts DC. Evolutionary disequilibrium among Indo-Pacific corals. Bulletin of Marine Science 1983, 33:619-632.
59. de Queiroz K. Species concepts and species delimitation. Systematic Biology 2007, 56:879-886.
60. Rice WR. Analyzing table of statistical tests. Evolution 1989, 43:223-225.
61. Richmond RH, Hunter CL. Reproduction and recruitment of corals: comparisons among the Caribbean, the tropical Pacific and the Red Sea. Marine Ecology Progress Series 1990, 60:185-203.
62. Rodriguez-Lanetty M, Krupp D, Weis VM. Distinct ITS types of Symbiodinium in Clade C correlate to cnidarian/dinoflagellate specificity during symbiosis onset. Marine Ecology Progress Series 2004, 275:97-102.
63. Rowan R. Coral bleaching: thermal adaptation in reef coral symbionts. Nature 2004, 430:742.
64. Sampayo EM, Franceschinis L, Hoegh-Guldberg O, Dove S. Niche partitioning of symbiotic dinoflagellates. Molecular Ecology 2007, 16:3721-3733.
65. Sampayo EM, Ridgeway T, Bongaerts P, Hoegh-Gulberg O. Bleaching susceptibility and mortality of corals are determined by fine-scale differences in symbiont type. Proceedings of the National Academy of Sciences USA 2008, 105:10444-10449.
66. Sampayo EM, Dove S, LaJeunesse TC. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Molecular Ecology 2009, 18:500-519.
67. Santos SR, Gutiérrez-Rodríguez C, Lasker HR, Coffroth MA. Symbiodinium sp. associations in the gorgonian Pseudopterogorgia elisabethae in the Bahamas: high levels of genetic variability and population structure in symbiotic dinoflagellates. Marine Biology 2003, 143:111-120.
68. Savage AM, Trapido-Rosenthal H, Douglas AE. On the functional significance of molecular variation in Symbiodinium, the symbiotic algae of Cnidaria: photosynthetic response to irradiance. Marine Ecological Progress Series 2002, 244:27-37.
69. Schluter D. Ecology and the origin of species. Trends in Ecology and Evolution 2001, 16:372-380.
70. Seutin G, White BN, Boag PT. Preservation of avian blood and tissue samples for DNA analyses. Canadian Journal of Zoology 1991, 69:82-90.
71. Sheppard CRC. Physical environment of the Gulf relevant to marine pollution: an overview. Marine Pollution Bulletin 1983, 27:3-8.
72. Sheppard CRC. Predicted recurrences of mass coral mortality in the Indian Ocean. Nature 2003, 425:294-296.
73. Sheppard CRC, Harris A, Sheppard ALS. Archipelago-wide coral reef recovery patterns since 1998 in the Chagos archipelago, central Indian Ocean. Marine Ecology Progress Series 2008, 362:109-117.
74. Sotka EE, Thacker RW. Do some corals like it hot? Trends in Ecology and Evolution 2005, 20:59-62.
75. Stat M, Loh WK, Hoegh-Guldberg O, Carter DA. Host symbiont acquisition strategy drives Symbiodinium diversity in the southern Great Barrier Reef. Coral Reefs 2008, 27:763-772.
76. Suggett DJ, Warner ME, Smith DJ, Davey P, Hennige SJ, Baker NR. Photosynthesis and accumulation of hydrogen peroxide by Symbiodinium (Pyrrhophyta) phylotypes with different thermal tolerances. Journal of Phycology 2008, 44:948-956.
77. Swofford DL. PAUP*. Phylogenetic analysis using parsimony (*and other methods), version 4.0b10 2000, Sinauer, Sunderland, MA
78. Tchernov D, Gorbunov MY, de Vargas C, Yadav SN, Vardi A, Häggblom M, Falkowski P. Membrane lipids of symbiotic algae are diagnostic of sensitivity to thermal bleaching in corals. Proceedings of the National Academy of Sciences USA 2004, 101:13531-13535.
79. Thornhill DJ, Fitt WK, Schmidt GW. Highly stable symbioses among western Atlantic brooding corals. Coral Reefs 2006a, 25:515-519.
80. Thornhill DJ, LaJeunesse TC, Kemp DW, Fitt WK, Schmidt GW. Multi-year seasonal genotypic surveys of coral-algal symbiosis reveal prevalent stability or post-bleaching reversion. Marine Biology 2006b, 148:711-722.
81. Thornhill DJ, LaJeunesse TC, Santos SR. Measuring rDNA diversity in eukaryotic microbial systems: how intragenomic variation, pseudogenes, and PCR artifacts confound biodiversity estimates. Molecular Ecology 2007, 16:5326-5340.
82. Thornhill DJ, Kemp DW, Bruns BU, Fitt WK, Schmidt GW. Correspondence between cold tolerance and temperate biogeography in a western Atlantic Symbiodinium (Dinophyta) lineage. Journal of Phycology 2008, 44:1126-1135.
83. Trench RK. Microalgal-invertebrate symbioses: a review. Endocytobiosis and Cell Research 1993, 9:135-175.
84. Trench RK, Blank RJ. Symbiodinium microadriaticum Freudenthal, S. goreauii sp. nov., S. kawagutii sp. nov. and S. pilosum sp. nov.: gymnodinioid dinoflagellate symbionts of marine invertebrates. Journal of Phycology 1987, 23:469-481.
85. Ulstrup KE, van Oppen MJH. Geographic and habitat partitioning of genetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the Great Barrier Reef. Molecular Ecology 2003, 12:3477-3484.
86. Visram S, Douglas AE. Molecular diversity of symbiotic algae (zooxanthellae) in scleractinian corals of Kenya. Coral Reefs 2006, 25:172-176.
87. Voris HK. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 2000, 27:1153-1167.
88. Wilkinson CR. Status of coral reefs of the world: 2000 2000, Australian Institute of Marine Science, Townsville
89. Wood R. The ecological evolution of reefs. Annual Review of Ecology, Evolution, and Systematics 1998, 29:179-206.